Chikungunya virus nsP3 & nsP4 interacts with HSP-90 to promote virus replication: HSP-90 inhibitors reduce CHIKV infection and inflammation in vivo

Antiviral Research

Volumn 103, Issue 1, 2014, Pages 7-16

  Rathore, Abhay P S ^a,b   Haystead, Timothy ^c   Das, Pratyush K ^d   Merits, Andres ^d   Ng, Mah Lee ^b   Vasudevan, Subhash G ^a,b  

^a DUKE NUS MEDICAL SCHOOL   (Singapore)

^b NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^c DUKE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d UNIVERSITY OF TARTU   (Estonia)

Author keywords

CHIKV mouse model; CHIKV nsP3; CHIKV nsP4; Geldanamycin; HSP 90; Protein interactions

Indexed keywords

ANTIVIRUS AGENT; CHAPERONE; CHIKUNGUNYA VIRUS NSP 3 PROTEIN; CHIKUNGUNYA VIRUS NSP 4 PROTEIN; GELDANAMYCIN; HEAT SHOCK PROTEIN 90; HEAT SHOCK PROTEIN 90 INHIBITOR; HS 100010; SMALL INTERFERING RNA; SNX 2112; UNCLASSIFIED DRUG; VIRUS PROTEIN; VIRUS RNA;

ANIMAL CELL; ARTICLE; BINDING SITE; CELL CULTURE; CHIKUNGUNYA; CHIKUNGUNYA ALPHAVIRUS; COMPARATIVE STUDY; CONFORMATION; CONTROLLED STUDY; DRUG INHIBITION; GENE SILENCING; HOST; HUMAN; HUMAN CELL; IN VIVO STUDY; INFECTION CONTROL; INFLAMMATION; MONONUCLEAR CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN INTERACTION; STRESS; TISSUE INJURY; VIREMIA; VIRUS REPLICATION;

CHIKV MOUSE MODEL; CHIKV NSP3; CHIKV NSP4; GELDANAMYCIN; HSP-90; PROTEIN INTERACTIONS;

ALPHAVIRUS INFECTIONS; ANIMALS; ANTIVIRAL AGENTS; CELL LINE; CENTRIFUGATION; CHIKUNGUNYA VIRUS; DISEASE MODELS, ANIMAL; ENZYME INHIBITORS; HOST-PATHOGEN INTERACTIONS; HSP90 HEAT-SHOCK PROTEINS; HUMANS; MASS SPECTROMETRY; MICE; OPTICAL IMAGING; PROTEIN BINDING; PROTEIN INTERACTION MAPPING; TREATMENT OUTCOME; VIRAL NONSTRUCTURAL PROTEINS; VIRUS REPLICATION;

EID: 84892658102     PISSN: 01663542     EISSN: 18729096     Source Type: Journal    
DOI: 10.1016/j.antiviral.2013.12.010     Document Type: Article

References (34)

1. M.M. Ali, S.M. Roe, C.K. Vaughan, P. Meyer, B. Panaretou, P.W. Piper, C. Prodromou, and L.H. Pearl Crystal structure of an Hsp90-nucleotide-p23/Sba1 closed chaperone complex Nature 440 2006 1013 1017
2. W.M. Bodnar, R.K. Blackburn, J.M. Krise, and M.A. Moseley Exploiting the complementary nature of LC/MALDI/MS/MS and LC/ESI/MS/MS for increased proteome coverage J. Am. Soc. Mass Spectrom. 14 2003 971 979 (Pubitemid 37040758)
3. G. Borgherini, P. Poubeau, F. Staikowsky, M. Lory, N. Le Moullec, J.P. Becquart, C. Wengling, A. Michault, and F. Paganin Outbreak of Chikungunya on Reunion Island: early clinical and laboratory features in 157 adult patients Clin. Infect. Dis. 44 2007 1401 1407 (Pubitemid 46801580)
4. M. Bourai, M. Lucas-Hourani, H.H. Gad, C. Drosten, Y. Jacob, L. Tafforeau, P. Cassonnet, L.M. Jones, D. Judith, T. Couderc, M. Lecuit, P. Andre, B.M. Kummerer, V. Lotteau, P. Despres, F. Tangy, and P.O. Vidalain Mapping of Chikungunya virus interactions with host proteins identified nsP2 as a highly connected viral component J. Virol. 86 2012 3121 3134
5. F.J. Burt, M.S. Rolph, N.E. Rulli, S. Mahalingam, and M.T. Heise Chikungunya: a re-emerging virus Lancet 379 2012 662 671
6. A. Chadli, I. Bouhouche, W. Sullivan, B. Stensgard, N. McMahon, M.G. Catelli, and D.O. Toft Dimerization and N-terminal domain proximity underlie the function of the molecular chaperone heat shock protein 90 Proc. Natl. Acad. Sci. USA 97 2000 12524 12529
7. B. Chen, W.H. Piel, L. Gui, E. Bruford, and A. Monteiro The HSP90 family of genes in the human genome: insights into their divergence and evolution Genomics 86 2005 627 637 (Pubitemid 41752943)
8. I.M. Cristea, H. Rozjabek, K.R. Molloy, S. Karki, L.L. White, C.M. Rice, M.P. Rout, B.T. Chait, and M.R. MacDonald Host factors associated with the Sindbis virus RNA-dependent RNA polymerase: role for G3BP1 and G3BP2 in virus replication J. Virol. 84 2010 6720 6732
9. P. Fadden, K.H. Huang, J.M. Veal, P.M. Steed, A.F. Barabasz, B. Foley, M. Hu, J.M. Partridge, J. Rice, A. Scott, L.G. Dubois, T.A. Freed, M.A. Silinski, T.E. Barta, P.F. Hughes, A. Ommen, W. Ma, E.D. Smith, A.W. Spangenberg, J. Eaves, G.J. Hanson, L. Hinkley, M. Jenks, M. Lewis, J. Otto, G.J. Pronk, K. Verleysen, T.A. Haystead, and S.E. Hall Application of chemoproteomics to drug discovery: identification of a clinical candidate targeting hsp90 Chem. Biol. 17 2010 686 694
10. R. Geller, S. Taguwa, and J. Frydman Broad action of Hsp90 as a host chaperone required for viral replication Biochim. Biophys. Acta 1823 2012 698 706
11. J.J. Hoarau, M.C. Jaffar Bandjee, P. Krejbich Trotot, T. Das, G. Li-Pat-Yuen, B. Dassa, M. Denizot, E. Guichard, A. Ribera, T. Henni, F. Tallet, M.P. Moiton, B.A. Gauzere, S. Bruniquet, Z. Jaffar Bandjee, P. Morbidelli, G. Martigny, M. Jolivet, F. Gay, M. Grandadam, H. Tolou, V. Vieillard, P. Debre, B. Autran, and P. Gasque Persistent chronic inflammation and infection by Chikungunya arthritogenic alphavirus in spite of a robust host immune response J. Immunol. 184 2010 5914 5927
12. J. Hu, and D. Anselmo In vitro reconstitution of a functional duck hepatitis B virus reverse transcriptase: posttranslational activation by Hsp90 J. Virol. 74 2000 11447 11455 (Pubitemid 32222291)
13. J. Hu, D.O. Toft, and C. Seeger Hepadnavirus assembly and reverse transcription require a multi-component chaperone complex which is incorporated into nucleocapsids EMBO J. 16 1997 59 68 (Pubitemid 27032850)
14. K.H. Huang, J.M. Veal, R.P. Fadden, J.W. Rice, J. Eaves, J.P. Strachan, A.F. Barabasz, B.E. Foley, T.E. Barta, W. Ma, M.A. Silinski, M. Hu, J.M. Partridge, A. Scott, L.G. DuBois, T. Freed, P.M. Steed, A.J. Ommen, E.D. Smith, P.F. Hughes, A.R. Woodward, G.J. Hanson, W.S. McCall, C.J. Markworth, L. Hinkley, M. Jenks, L. Geng, M. Lewis, J. Otto, B. Pronk, K. Verleysen, and S.E. Hall Discovery of novel 2-aminobenzamide inhibitors of heat shock protein 90 as potent, selective and orally active antitumor agents J. Med. Chem. 52 2009 4288 4305
15. P.F. Hughes, J.J. Barrott, D.A. Carlson, D.R. Loiselle, B.L. Speer, K. Bodoor, L.A. Rund, and T.A. Haystead A highly selective Hsp90 affinity chromatography resin with a cleavable linker Bioorg. Med. Chem. 20 2012 3298 3305
16. P. Kaur, and J.J. Chu Chikungunya virus: an update on antiviral development and challenges Drug Discov. Today 18 2013 969 983
17. S.P. Lees-Miller, and C.W. Anderson The human double-stranded DNA-activated protein kinase phosphorylates the 90-kDa heat-shock protein, hsp90 alpha at two NH2-terminal threonine residues J. Biol. Chem. 264 1989 17275 17280 (Pubitemid 19255559)
18. L. Li, J. Jose, Y. Xiang, R.J. Kuhn, and M.G. Rossmann Structural changes of envelope proteins during alphavirus fusion Nature 468 2010 705 708
19. E. Little, M. Ramakrishnan, B. Roy, G. Gazit, and A.S. Lee The glucose-regulated proteins (GRP78 and GRP94): functions, gene regulation, and applications Crit. Rev. Eukaryot. Gene Expr. 4 1994 1 18 (Pubitemid 24238439)
20. V. Lulla, D.Y. Kim, E.I. Frolova, and I. Frolov The amino-terminal domain of alphavirus capsid protein is dispensable for viral particle assembly, but regulates RNA encapsidation through cooperative function of its subdomains J. Virol. 87 2013 12003 12019
21. X. Meng, J. Devin, W.P. Sullivan, D. Toft, E.E. Baulieu, and M.G. Catelli Mutational analysis of Hsp90 alpha dimerization and subcellular localization: dimer disruption does not impede "in vivo" interaction with estrogen receptor J. Cell Sci. 109 Pt 7 1996 1677 1687 (Pubitemid 26248613)
22. F. Momose, T. Naito, K. Yano, S. Sugimoto, Y. Morikawa, and K. Nagata Identification of Hsp90 as a stimulatory host factor involved in influenza virus RNA synthesis J. Biol. Chem. 277 2002 45306 45314 (Pubitemid 36159137)
23. T. Naito, F. Momose, A. Kawaguchi, and K. Nagata Involvement of Hsp90 in assembly and nuclear import of influenza virus RNA polymerase subunits J. Virol. 81 2007 1339 1349 (Pubitemid 46167855)
24. T. Okamoto, Y. Nishimura, T. Ichimura, K. Suzuki, T. Miyamura, T. Suzuki, K. Moriishi, and Y. Matsuura Hepatitis C virus RNA replication is regulated by FKBP8 and Hsp90 EMBO J. 25 2006 5015 5025 (Pubitemid 44607045)
25. L.H. Pearl, and C. Prodromou Structure and mechanism of the Hsp90 molecular chaperone machinery Annu. Rev. Biochem. 75 2006 271 294 (Pubitemid 44118034)
26. C. Prodromou, B. Panaretou, S. Chohan, G. Siligardi, R. O'Brien, J.E. Ladbury, S.M. Roe, P.W. Piper, and L.H. Pearl The ATPase cycle of Hsp90 drives a molecular 'clamp' via transient dimerization of the N-terminal domains EMBO J. 19 2000 4383 4392 (Pubitemid 30623749)
27. A.A. Rashad, S. Mahalingam, and P.A. Keller Chikungunya virus: emerging targets and new opportunities for medicinal chemistry J. Med. Chem. 2013
28. A.P. Rathore, M.L. Ng, and S.G. Vasudevan Differential unfolded protein response during Chikungunya and Sindbis virus infection: CHIKV nsP4 suppresses eIF2alpha phosphorylation Virol. J. 10 2013 36
29. A.P. Rathore, P.N. Paradkar, S. Watanabe, K.H. Tan, C. Sung, J.E. Connolly, J. Low, E.E. Ooi, and S.G. Vasudevan Celgosivir treatment misfolds dengue virus NS1 protein, induces cellular pro-survival genes and protects against lethal challenge mouse model Antiviral Res. 92 2011 453 460
30. O. Schwartz, and M.L. Albert Biology and pathogenesis of Chikungunya virus Nat. Rev. Microbiol. 8 2010 491 500
31. C.E. Stebbins, A.A. Russo, C. Schneider, N. Rosen, F.U. Hartl, and N.P. Pavletich Crystal structure of an Hsp90-geldanamycin complex: targeting of a protein chaperone by an antitumor agent Cell 89 1997 239 250 (Pubitemid 27199896)
32. J.H. Strauss, and E.G. Strauss The alphaviruses: gene expression, replication, and evolution Microbiol. Rev. 58 1994 491 562
33. M. Varjak, S. Saul, L. Arike, A. Lulla, L. Peil, and A. Merits Magnetic fractionation and proteomic dissection of cellular organelles occupied by the late replication complexes of semliki forest virus J. Virol. 87 2013 10295 10312
34. J.E. Voss, M.C. Vaney, S. Duquerroy, C. Vonrhein, C. Girard-Blanc, E. Crublet, A. Thompson, G. Bricogne, and F.A. Rey Glycoprotein organization of Chikungunya virus particles revealed by X-ray crystallography Nature 468 2010 709 712